A New Species of Tapir from the Amazon Author(S): Mario A
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A new species of tapir from the Amazon Author(s): Mario A. Cozzuol , Camila L. Clozato , Elizete C. Holanda , Flávio H. G. Rodrigues , Samuel Nienow , Benoit de Thoisy , Rodrigo A. F. Redondo , and Fabrício R. Santos Source: Journal of Mammalogy, 94(6):1331-1345. 2013. Published By: American Society of Mammalogists DOI: http://dx.doi.org/10.1644/12-MAMM-A-169.1 URL: http://www.bioone.org/doi/full/10.1644/12-MAMM-A-169.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Mammalogy, 94(6):1331–1345, 2013 A new species of tapir from the Amazon MARIO A. COZZUOL,* CAMILA L. CLOZATO,ELIZETE C. HOLANDA,FLA´ VIO H. G. RODRIGUES,SAMUEL NIENOW, BENOIT DE THOISY,RODRIGO A. F. REDONDO, AND FABRICIO´ R. SANTOS* Universidade Federal de Minas Gerais, Avenida Antonio Carlos 6627, Belo Horizonte, Minas Gerais, Brazil (MAC, CLC, FHGR, RAFR, FRS) Universidade Federal do Rio Grande do Sul and Funda¸ca˜o Zoobotanicaˆ do Rio Grande do Sul, R. Dr. Salvador Fran¸ca, 1427, Porto Alegre, Rio Grande do Sul, Brazil (ECH) Instituto Pro-Carn´ ´ıvoros, Avenida Hora´cio Neto, 1030, Atibaia, Sa˜o Paulo, Brazil (FHGR) Instituto Chico Mendes de Biodiversidade, Avenida Dr. Mendon¸ca Lima 481, Guajara´-Mirim, Rondoˆnia, Brazil (SN) Kwata NGO & Institut Pasteur de la Guyane, 23 Avenue Pasteur, Cayenne, French Guiana (BdeT) Institute of Science and Technology, Am Campus 1, 3400, Klosterneuburg, Austria (RAFR) * Correspondents: [email protected], [email protected] All known species of extant tapirs are allopatric: 1 in southeastern Asia and 3 in Central and South America. The fossil record for tapirs, however, is much wider in geographical range, including Europe, Asia, and North and South America, going back to the late Oligocene, making the present distribution a relict of the original one. We here describe a new species of living Tapirus from the Amazon rain forest, the 1st since T. bairdii Gill, 1865, and the 1st new Perissodactyla in more than 100 years, from both morphological and molecular characters. It is shorter in stature than T. terrestris (Linnaeus, 1758) and has distinctive skull morphology, and it is basal to the clade formed by T. terrestris and T. pinchaque (Roulin, 1829). This highlights the unrecognized biodiversity in western Amazonia, where the biota faces increasing threats. Local peoples have long recognized our new species, suggesting a key role for traditional knowledge in understanding the biodiversity of the region. Key words: Amazon, biodiversity, cladistics, genetics, morphometry, new species, Tapirus Ó 2013 American Society of Mammalogists DOI: 10.1644/12-MAMM-A-169.1 The known living tapirs inhabit southeastern Asia, Central are preferred food for local human populations and are actors in America, and South America (Nowak 1997). Extant tapir the traditional beliefs of Amerindian communities (Nowak diversity and distribution are relicts of a richer group of species 1997; International Union for the Conservation of Nature and and larger distribution range attained during the Pleistocene Natural Resources 2009). (Simpson 1945; Nowak 1997; Hulbert 1999; Holanda et al. Here we describe a 5th living species of Tapirus, the 4th in 2011). Despite some controversies (Hershkovitz 1954), the 4 the Neotropics, the 1st since T. bairdii Gill, 1865, one of the living and many fossil species from Eurasia and the Americas largest land mammals recently described, and the only new are all placed in the genus Tapirus (Simpson 1945; Perissodactyla in more than 100 years (Ceballos and Ehlrich Hershkovitz 1954; Yingjun and Gaunfu 1987; Hulbert 1999; 2009). Despite popular accounts of the occurrence of more than Spassov and Ginsburg 1999; Holanda and Cozzuol 2006; 1 tapir species in lowland Amazonia, it was assumed that Ferrero and Noriega 2007; Holanda et al. 2011). Tapirs reached observed diversity of both morphological (Hershkovitz 1954) South America during the Great American Biotic Interchange, and molecular (de Thoisy et al. 2010) characters represented where they survived the late Pleistocene extinction, as the variations of T. terrestris (Linnaeus, 1758). We present here largest living terrestrial mammal on the continent (Woodburne detailed morphological and molecular (mitochondrial DNA 2010). All extant species are currently considered to be [mtDNA]) comparisons of specimens from western Brazilian vulnerable or endangered, by overhunting and habitat destruc- Amazon with all other Tapirus species, which indicate the tion (International Union for the Conservation of Nature and Natural Resources 2009). As seed predators and dispersers, they have key roles in the dynamics of rain forests, Cerrado, Pantanal, and high mountain ecosystems (Olmos 1997). They www.mammalogy.org 1331 1332 JOURNAL OF MAMMALOGY Vol. 94, No. 6 presence of this new taxon. Our study includes the largest Molecular phylogenetic analyses.—The following total geographic sampling of T. terrestris so far attempted. sample numbers, or sequences, or both, were included in the analyses: T. terrestris: n ¼ 52, T. bairdii: n ¼ 3, T. pinchaque: n ¼ 5, T. indicus: n ¼ 4, Tapirus sp. nov.: n ¼ 4. Equus caballus MATERIALS AND METHODS or Rhinocerotidae, or both, were used as out-groups. Samples.—Skull samples and measures were obtained from The DNA sequences from 3 mtDNA genes (cytochrome b specimens in museum collections, those collected in the field, [Cytb], cytochrome oxidase I [COI], and cytochrome oxidase II or animals provided by indigenous hunters. Skull and tissue [COII]) from living Tapirus species were generated and samples obtained from collected specimens in Brazil were compared to previously published data (Ashley et al. 1996; approved by Ministerio´ do Meio Ambiente, Sistema de Norman and Ashley 2000; de Thoisy et al. 2010). We included Autoriza¸ca˜o e Informa¸ca˜o em Biodiversidade—SISBIO a thorough analysis of the Cytb in a large geographic sampling (number: 21055-2; issue date: 11 December 2009). No in South America, such as has been shown to be useful in permit was required for field sampling carried out in French recovering mammalian phylogeny and exposing cryptic species Guiana. A sample of Tapirus indicus, Desmarest, 1819, was (Baker and Bradley 2006; Redondo et al. 2008). Sequence provided by the San Diego Zoo, San Diego, California. alignments were performed using Clustal W 2.1 (Larkin et al. Sequence data for other specimens and species from different 2007) and edited or concatenated, or both, when necessary with countries were retrieved from GenBank (Benson et al. 2005), the Alignment Explorer function implemented in MEGA 5.1 or published elsewhere (de Thoisy et al. 2010). (Tamura et al. 2011). The resulting alignments were used in Morphological studies.—Canonical variate analysis phylogenetic reconstructions by 2 methods. First, a maximum- (multivariate analysis of variance [MANOVA]–canonical likelihood search was performed in PhyML 3.0.1 (Guindon et variate analysis [CVA]) of 22 cranial measurements al. 2010) using the GTRþCþinv model with parameters (Supporting Information S1, DOI: 10.1644/ estimated from the data by the maximum-likelihood approach. 12-MAMM-A-169.S1) was performed with the software The initial tree was a BioNJ tree and the search was performed PAST version 2.14 (Hammer et al. 2001), using the using both NNI and SPR rearrangements in each interaction Hotelling’s Bonferroni-corrected option to test the keeping only the tree with best likelihood score. After a full discrimination of each of the species. Data were available for PhyML search on tree topology and parameters, the maximum- likelihood tree was used again as an initial tree for a new run all living species: T. terrestris: n ¼ 52, T. indicus: n ¼ 3, T. and the search was repeated until no significant gain in bairdii: n ¼ 4, T. pinchaque (Roulin, 1829): n ¼ 3, Tapirus sp. likelihood was observed in a likelihood-ratio test. The nov.: n ¼ 8 (for a list of the specimens see Supporting confidence in the clades was assessed through the approximate Information S2, DOI: 10.1644/12-MAMM-A-169.S2). Some likelihood-ratio (aLRT) test (Anisimova and Gascuel 2006; fossil species were included, which represent all of the South Anisimova et al. 2011). Second, we used a Bayesian inference American and several North American taxa known from skulls method with MrBayes 3.2.1 (Ronquist et al. 2011) using a complete enough to take most, if not all, the measurements GTRþCþinv model of nucleotide evolution and assuming flat used. Although some skulls of Tapirus sp. nov. collected by Dirichlet priors for parameter estimates and unconstrained the Karitiana Indians were partially damaged, so some branch lengths. The search was carried out using 2 independent measurements are missing, they were included in some of the runs of 4 Markov chains (1 cold and 3 heated) for 3 3 106 analyses. Qualitative comparison of discrete characters was generations, sampling every 300 generations with a burn-in of derived from available specimens, museum collections, and the 25% of the samples for the estimates of topology and literature. A figure including the measurements, their parameters. Stationarity of the chains was checked by plotting descriptions, and a list of specimens used in the analyses are parameters against generation in Tracer 1.5 (Rambaut and provided in Supporting Information S1 and S2.